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The Lifestyle of the Segmented Filamentous Bacterium: A Non-Culturable Gut-Associated Immunostimulating Microbe Inferred by Whole-Genome Sequencing

Numerous microbes inhabit the mammalian intestinal track and strongly impact host physiology; however, our understanding of this ecosystem remains limited owing to the high complexity of the microbial community and the presence of numerous non-culturable microbes. Segmented filamentous bacteria (SFB...

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Autores principales: Kuwahara, Tomomi, Ogura, Yositoshi, Oshima, Kenshiro, Kurokawa, Ken, Ooka, Tadasuke, Hirakawa, Hideki, Itoh, Takehiko, Nakayama-Imaohji, Haruyuki, Ichimura, Minoru, Itoh, Kikuji, Ishifune, Chieko, Maekawa, Yoichi, Yasutomo, Koji, Hattori, Masahira, Hayashi, Tetsuya
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3158464/
https://www.ncbi.nlm.nih.gov/pubmed/21791478
http://dx.doi.org/10.1093/dnares/dsr022
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author Kuwahara, Tomomi
Ogura, Yositoshi
Oshima, Kenshiro
Kurokawa, Ken
Ooka, Tadasuke
Hirakawa, Hideki
Itoh, Takehiko
Nakayama-Imaohji, Haruyuki
Ichimura, Minoru
Itoh, Kikuji
Ishifune, Chieko
Maekawa, Yoichi
Yasutomo, Koji
Hattori, Masahira
Hayashi, Tetsuya
author_facet Kuwahara, Tomomi
Ogura, Yositoshi
Oshima, Kenshiro
Kurokawa, Ken
Ooka, Tadasuke
Hirakawa, Hideki
Itoh, Takehiko
Nakayama-Imaohji, Haruyuki
Ichimura, Minoru
Itoh, Kikuji
Ishifune, Chieko
Maekawa, Yoichi
Yasutomo, Koji
Hattori, Masahira
Hayashi, Tetsuya
author_sort Kuwahara, Tomomi
collection PubMed
description Numerous microbes inhabit the mammalian intestinal track and strongly impact host physiology; however, our understanding of this ecosystem remains limited owing to the high complexity of the microbial community and the presence of numerous non-culturable microbes. Segmented filamentous bacteria (SFBs), which are clostridia-related Gram-positive bacteria, are among such non-culturable populations and are well known for their unique morphology and tight attachment to intestinal epithelial cells. Recent studies have revealed that SFBs play crucial roles in the post-natal maturation of gut immune function, especially the induction of Th17 lymphocytes. Here, we report the complete genome sequence of mouse SFBs. The genome, which comprises a single circular chromosome of 1 620 005 bp, lacks genes for the biosynthesis of almost all amino acids, vitamins/cofactors and nucleotides, but contains a full set of genes for sporulation/germination and, unexpectedly, for chemotaxis/flagella-based motility. These findings suggest a triphasic lifestyle of the SFB, which comprises two types of vegetative (swimming and epicellular parasitic) phases and a dormant (spore) phase. Furthermore, SFBs encode four types of flagellin, three of which are recognized by Toll-like receptor 5 and could elicit the innate immune response. Our results reveal the non-culturability, lifestyle and immunostimulation mechanisms of SFBs and provide a genetic basis for the future development of the SFB cultivation and gene-manipulation techniques.
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spelling pubmed-31584642011-08-19 The Lifestyle of the Segmented Filamentous Bacterium: A Non-Culturable Gut-Associated Immunostimulating Microbe Inferred by Whole-Genome Sequencing Kuwahara, Tomomi Ogura, Yositoshi Oshima, Kenshiro Kurokawa, Ken Ooka, Tadasuke Hirakawa, Hideki Itoh, Takehiko Nakayama-Imaohji, Haruyuki Ichimura, Minoru Itoh, Kikuji Ishifune, Chieko Maekawa, Yoichi Yasutomo, Koji Hattori, Masahira Hayashi, Tetsuya DNA Res Full Papers Numerous microbes inhabit the mammalian intestinal track and strongly impact host physiology; however, our understanding of this ecosystem remains limited owing to the high complexity of the microbial community and the presence of numerous non-culturable microbes. Segmented filamentous bacteria (SFBs), which are clostridia-related Gram-positive bacteria, are among such non-culturable populations and are well known for their unique morphology and tight attachment to intestinal epithelial cells. Recent studies have revealed that SFBs play crucial roles in the post-natal maturation of gut immune function, especially the induction of Th17 lymphocytes. Here, we report the complete genome sequence of mouse SFBs. The genome, which comprises a single circular chromosome of 1 620 005 bp, lacks genes for the biosynthesis of almost all amino acids, vitamins/cofactors and nucleotides, but contains a full set of genes for sporulation/germination and, unexpectedly, for chemotaxis/flagella-based motility. These findings suggest a triphasic lifestyle of the SFB, which comprises two types of vegetative (swimming and epicellular parasitic) phases and a dormant (spore) phase. Furthermore, SFBs encode four types of flagellin, three of which are recognized by Toll-like receptor 5 and could elicit the innate immune response. Our results reveal the non-culturability, lifestyle and immunostimulation mechanisms of SFBs and provide a genetic basis for the future development of the SFB cultivation and gene-manipulation techniques. Oxford University Press 2011-08 2011-07-26 /pmc/articles/PMC3158464/ /pubmed/21791478 http://dx.doi.org/10.1093/dnares/dsr022 Text en © The Author 2011. Published by Oxford University Press on behalf of Kazusa DNA Research Institute. http://creativecommons.org/licenses/by-nc/2.5/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.5), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Full Papers
Kuwahara, Tomomi
Ogura, Yositoshi
Oshima, Kenshiro
Kurokawa, Ken
Ooka, Tadasuke
Hirakawa, Hideki
Itoh, Takehiko
Nakayama-Imaohji, Haruyuki
Ichimura, Minoru
Itoh, Kikuji
Ishifune, Chieko
Maekawa, Yoichi
Yasutomo, Koji
Hattori, Masahira
Hayashi, Tetsuya
The Lifestyle of the Segmented Filamentous Bacterium: A Non-Culturable Gut-Associated Immunostimulating Microbe Inferred by Whole-Genome Sequencing
title The Lifestyle of the Segmented Filamentous Bacterium: A Non-Culturable Gut-Associated Immunostimulating Microbe Inferred by Whole-Genome Sequencing
title_full The Lifestyle of the Segmented Filamentous Bacterium: A Non-Culturable Gut-Associated Immunostimulating Microbe Inferred by Whole-Genome Sequencing
title_fullStr The Lifestyle of the Segmented Filamentous Bacterium: A Non-Culturable Gut-Associated Immunostimulating Microbe Inferred by Whole-Genome Sequencing
title_full_unstemmed The Lifestyle of the Segmented Filamentous Bacterium: A Non-Culturable Gut-Associated Immunostimulating Microbe Inferred by Whole-Genome Sequencing
title_short The Lifestyle of the Segmented Filamentous Bacterium: A Non-Culturable Gut-Associated Immunostimulating Microbe Inferred by Whole-Genome Sequencing
title_sort lifestyle of the segmented filamentous bacterium: a non-culturable gut-associated immunostimulating microbe inferred by whole-genome sequencing
topic Full Papers
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3158464/
https://www.ncbi.nlm.nih.gov/pubmed/21791478
http://dx.doi.org/10.1093/dnares/dsr022
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